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Ecotoxicology and Public Health

Respiratory Aerosol Emissions from Vocalization: Age and Sex Differences Are Explained by Volume and Exhaled CO2
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  • Nicholas Good
    Nicholas Good
    Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, Colorado 80523, United States
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  • Kristen M. Fedak
    Kristen M. Fedak
    Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, Colorado 80523, United States
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  • Dan Goble
    Dan Goble
    School of Music, Theatre, and Dance, Colorado State University, Fort Collins, Colorado 80523, United States
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  • Amy Keisling
    Amy Keisling
    School of Music, Theatre, and Dance, Colorado State University, Fort Collins, Colorado 80523, United States
    Mechanical Engineering, Colorado State University, Fort Collins, Colorado 80523, United States
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  • Christian L’Orange
    Christian L’Orange
    Mechanical Engineering, Colorado State University, Fort Collins, Colorado 80523, United States
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  • Emily Morton
    Emily Morton
    School of Music, Theatre, and Dance, Colorado State University, Fort Collins, Colorado 80523, United States
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  • Rebecca Phillips
    Rebecca Phillips
    School of Music, Theatre, and Dance, Colorado State University, Fort Collins, Colorado 80523, United States
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  • Ky Tanner
    Ky Tanner
    Mechanical Engineering, Colorado State University, Fort Collins, Colorado 80523, United States
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  • John Volckens*
    John Volckens
    Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, Colorado 80523, United States
    Mechanical Engineering, Colorado State University, Fort Collins, Colorado 80523, United States
    *Email: [email protected]. Phone: 970-491-6341. Corresponding author address: Department of Mechanical Engineering, Campus Delivery 1374, Colorado State University, Fort Collins, CO, 80521 USA.
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    Orcidhttps://orcid.org/0000-0002-7563-9525
Open PDFSupporting Information (1)

Environmental Science & Technology Letters

Cite this: Environ. Sci. Technol. Lett. 2021, 8, 12, 1071–1076
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https://doi.org/10.1021/acs.estlett.1c00760
Published November 9, 2021

Copyright © 2021 The Authors. Published by American Chemical Society. This publication is licensed under

CC-BY-NC-ND 4.0 .

Abstract

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Evidence suggests that airborne transmission of infectious respiratory aerosol plays an important role for the SARS-CoV-2 virus. This work characterized respiratory aerosol emissions from a panel of healthy individuals of varying age and sex while talking and singing in a controlled laboratory setting. Particle number concentrations between 0.25 and 33 μm were measured from 63 participants aged 12–61 years with concurrent monitoring of voice volume and exhaled CO2 levels. On average, singing produced 77% (95% CI: 42,109%) more aerosol than talking, adults produced 62% (CI: 27,98%) more aerosol than minors, and males produced 34% (CI: 0,70%) more aerosol than females. After accounting for participant voice volume and exhaled CO2 (both of which were positively correlated with aerosol emissions) in linear models, the age and sex differences were attenuated and no longer statistically significant. These results support further investigation of voice volume and CO2 as indicators of infection risk indoors.

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Copyright © 2021 The Authors. Published by American Chemical Society

Introduction

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The recent COVID-19 pandemic has raised awareness to the lack of scientific understanding surrounding human respiratory aerosol generation and disease transmission. Activities like sneezing, coughing, talking, and breathing produce respiratory aerosols–airborne mucosalivary particles with aerodynamic diameters less than 100 μm that emanate from the respiratory tract. Respiratory aerosols can carry pathogens and therefore play a key role in infectious disease transmission. (1−5)
Evidence suggests that the SARS-CoV-2 virus (which causes COVID-19) is transmitted via infectious respiratory aerosols (6−8) and at distances beyond 1.8 m (6 ft). (9) Strategies to reduce exposure risk are predicated on understanding the rate and variability of respiratory aerosol emissions as a function of various human activities. Without such information, public health authorities must make highly uncertain recommendations, which can result in the precautionary principle dictating policy. (10)
For example, a COVID-19 outbreak in March 2020 occurred among singers in Skagit County, Washington, USA, in which 53 of the 61 individuals who attended a single choir practice became infected, three were hospitalized, and two died. (11) As a result of this and similar outbreaks, along with mounting uncertainties about modes of transmission, the performing arts industry effectively shut down in 2020. Several studies have characterized aerosol emissions from nonvocal (i.e., breathing) and vocalization activities, (12−16) with volume playing a major role in emissions, (16) and activities like singing generating more aerosol than talking. (12,14,15,17) These studies, however, have generally been small in size and limited in scope, which limits population generalizability.
Therefore, we sought to characterize respiratory aerosol emissions from a large panel of individuals of varying age (and sex) while talking and singing, in a laboratory setting, to help elucidate the relative risks and potential for infection transmission from these activities. We modeled these emissions as a function of participant volume (sound pressure level) and exhaled CO2, as the latter has been proposed as an indicator of infection risk indoors. (18)

Materials and Methods

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Healthy volunteer performers aged 12 years and older were recruited to participate in the study (CSU IRB Approval, 20-10174H). Participants from four performance specialties were recruited (vocalists, actors, dancers, and woodwind/brass instrumentalists). Recruitment was targeted to provide equal blocks of minors (ages 12 to 18) and adults (ages 18 and older). Participants self-reported their demographic information, including age, height, weight, race, ethnicity, and sex assigned at birth via questionnaire.
Each participant completed a series of maneuvers specific to their specialty and ability level, along with two generic vocal maneuvers: talking and singing. This paper is focused on respiratory aerosol emissions from the generic vocal maneuvers, which were singing “Happy Birthday” and reading “The Caterpillar” (19) out loud at a conversational volume and style. The reading passage was chosen because it included a broad range of sound classes and articulations, while maintaining simple syntax. Each vocal maneuver was repeated continuously over a period of 4 min, during which a single, time-averaged measurement was recorded.
Participants undertook the maneuvers inside a 3.45 m × 2.8 m × 2.45 m environmental chamber (20) ventilated with HEPA-filtered air. Chamber airflow was controlled, and environmental conditions (temperature, humidity) inside the chamber were logged along with all measurement data using LabVIEW (National Instruments, TX) instrument control and data acquisition software. A constant-volume sampling apparatus (10 L·min–1) was used to capture aerosol emissions from participants (Figure S2). To establish background particle levels, participants were asked to sit in a corner of the chamber, approximately 1.5 m from the sampling apparatus, while wearing a face mask.
Respiratory aerosol concentrations (between 0.25 and 33 μm) were measured by an optical particle counter (OPC; Model 11-D, Grimm Aerosol Technik, Germany) and are reported in terms of raw concentrations (i.e., particle concentration measured downstream of the participant within the sampling apparatus [particles·L–1 of sampled air]) and also in terms of exhaled concentrations (i.e., raw concentration scaled by the measured CO2 mixing ratio and standardized to estimate particles·L–1 of exhaled breath). Details of these calculations and related background corrections are provided in the Supporting Information.
We fit a linear model (Model 1) to explore the effect of maneuver, sex, and age on the raw respiratory aerosol concentrations. Maneuver (talking vs singing), sex (male vs female), and age (minor vs adult) were binary variables in the model

Model 1

(1)
where βi represents the effect estimate for each predictor in the model. We also fit a linear model (Model 2) to explore the effect of maneuver, sex, age, and sound pressure level on exhaled concentrations of respiratory aerosols

Model 2

(2)
where sound pressure (dBA) represents the A-weighted and z-scaled sound pressure level measured above each participant. (21) All data analyses were conducted in R (R Core Team, version 4.0.4).

Results and Discussion

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Emissions from vocal maneuvers were successfully collected from 63 participants. Forty-six percent of participants (n = 29) were female, defined as sex assigned at birth. Participants ranged from 12 to 61 years old (mean age 23 years); 27 participants were adults (age ≥18). Of the 63 participants, 11% (n = 7) had specific vocal training (acting and/or singing), while the remaining 89% (n = 56) were trained as instrumentalists.
Table 1 provides summary statistics for measured sound pressure, CO2 mixing ratio, and respiratory aerosol concentrations by maneuver and demographics. The volume, CO2, and raw concentration data reported here are endogenous to the measurement system (i.e., their magnitude depends on the experimental setup), whereas the exhaled concentration data are exogenous and, thus, more appropriate for generalization beyond the conditions reported here. However, because we sampled near-field emissions at a flow rate that approximates average human breathing (10 L·min–1), the raw concentration data reported here are likely to be representative of concentrations encountered in the near-field of human vocalization. Further, the relative differences between our observed variables (i.e., raw emissions by maneuver, age, and sex) are real, and those differences are unlikely to be affected by the system of measurement. We calculate respiratory aerosol emission rates (#·s–1) assuming a minute ventilation rate of 7.5 L·min–1.
Table 1. Descriptive Statistics for Sound Pressure, Carbon Dioxide (CO2), and Respiratory Aerosol Emissions as a Function of Maneuver and Participant Demographics
 talkingsingingadultsminorsmalefemale
 mean (min, max)IQRmean (min, max)IQRmean (min, max)IQRmean (min, max)IQRmean (min, max)IQRmean (min, max)IQR
sound pressure (dBA)67.5 (62.4, 73)3.970.0 (61.8, 77)6.270.3 (62.9, 77)5.3667.2 (61.8, 73.9)4.5967.3 (61.8, 77)3.270.0 (62.8, 77)4.32
CO2 (ppmV in air)3797 (573, 10125)21434122 (635, 9790)24494697 (635,10125)23273411 (573, 7087)23473310 (573, 5692)20554471 (641, 10125)2585
raw concn (#·L-1 air)142 (<50a, 547)144278 (<50, 937)233270 (<50, 937)274161 (<50, 727)108235 (<50, 848)111173 (<50, 937)205
exhaled concn (#·L-1 breath)1915 (<450a, 7269)15823289 (<450, 9551)23592825 (<450, 9551)21772390 (<450, 7297)16962515 (<450, 9551)16732646 (<450, 8253)1903
exhaled rate (#·s-1)239 (<56a, 909)198411 (<56, 1194)295353 (<56, 1194)272299 (<56, 912)212314 (<56, 1194)209331 (<56, 1032)238
a

Raw concentrations <50 particles·L–1 of air, exhaled concentrations <450 particles·L–1 of breath, and exhaled rates <56 particles·s–1 indicate concentrations below the method detection limits. All data are background corrected. IQR: interquartile range. The exhaled rate was calculated from exhaled concentration and assuming a minute ventilation rate of 7.5 L·min–1.

Raw Concentration Emissions

Shown in Figure 1 are raw concentration measurements as a function of age, sex, and maneuver. Despite the wide variation in respiratory aerosol emission rates within categories, important differences exist. In single-variable models, being adult, male, and singing (vs talking) produced a significant increase in raw respiratory aerosol emissions. In the multivariate model (Model 1 and Table S1), singing resulted in an increase of 133 particles·L–1 (95% CI: 73, 194) vs talking, being male resulted in an increase of 59 particles·L–1 (95% CI: 0, 120) vs being female, and being a minor resulted in a decrease of emissions of 107 particles·L–1 (95% CI: −168, −46) in the air immediately downstream of a participant. Alsved et al. (12) also measured aerosol emissions from 12 adults who were either professional or amateur trained singers; they reported that singing generated more particles than talking and that volume played a role in emissions. Our respiratory aerosol emissions agree with Johnson et al., who estimated a (raw) particle number concentration of 154·L–1 from talking (vs our study average estimate of 142·L–1; Table 1). Assuming a human breathing rate of 7.5 L·min–1, our mean emission rates for exhaled aerosol equate to 239 (range: 56–909) and 411 (56–1194) particles·s–1 from talking and singing, respectively (Table 1). These values overlap with those of Alsved et al., (12) who reported 270 (120–1380) and 690 (320–2870) particles·s–1 for adult talking and singing, respectively, and Mürbe et al. (14) who reported a range from 320 to 2870 particles·s–1 for adult singing. The aerosol size distribution reported by the OPC (Figure S7) was log-normal and bimodal, with one mode centered at 0.5 μm and the other at 1.3 μm, in approximate agreement for the breathing and laryngeal emission modes reported by Johnson et al. (22)

Figure 1

Figure 1. Raw respiratory aerosol concentrations (0.25–33 μm in diameter) measured across different populations and activities. Solid line represents the median, boxes delineate the IQR, and whiskers represent IQR·1.5 or the data minima. The horizontal, dashed line represents a method quantification limit of 50 particles·L–1. Participant data are shown as open circles.

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To investigate potential physiologic mechanisms behind the age and sex differences, we examined correlations between raw concentration emissions first with voice volume and then with exhaled CO2. Asadi et al. (16) demonstrated that voice volume was correlated with respiratory aerosol emissions from speech, which we confirm among our panel of 63 volunteers (r2 = 0.37; Figure S2). Increased sound pressure from vocalization is a result of more energy imparted to the vocal folds (in terms of vibrational amplitude), and this increase in vibrational energy from subglottal pressure (23) is likely the putative mechanism for increased probability of droplet release from the vocal folds. (22) Similar to Asadi et al., the strength of the correlation in Figure S4 is diminished due to the large person-to-person variability in base aerosol emissions from vocalization. This between-person variability is also evident in Figure 1.
We also observed a statistically significant correlation between raw concentrations and exhaled CO2 (r2 = 0.3; Figure S5), which we hypothesize is due to increased lung capacity (and hence, increased expiration) in both males and adults. These relationships are confirmed in Table S2, where being male, adult, and vocalizing at higher volume are all significantly associated with increases in exhaled CO2. The results are consistent with adults and males having larger vital lung capacity (i.e., the amount of air that can be forced out of the lungs in a single breath), on average, than minors and females (24,25) and, therefore, higher CO2 emission rates. We hypothesize that increased vital capacity presents more opportunity for the release of “fluid film burst” droplets (26,27) from the respiratory bronchioles upon exhalation (though this hypothesis remains untested). We note that vocal ability (defined as having professional vocal arts experience, n = 7/63 participants) was not associated with either CO2 or respiratory aerosol emissions, although our sample for this test was small (data not shown).

Exhaled Concentrations

Given that exhaled CO2 was associated with raw respiratory aerosol concentrations, we normalized each participant’s raw concentrations to their average CO2 emissions during a maneuver and then scaled these values to represent emissions per liter of exhaled breath (concentrationexhaled; shown in Figure S6). We then evaluated whether the effects of participant age and sex (both as binary variables) persisted in a linear model (Model 2) that included voice volume.
The results of this model, shown as percent increase relative to a reference case (or by one standard deviation increase in the case of sound pressure level), are provided in Figure 2 and Table S3. Interestingly, the sex and age effects on exhaled respiratory aerosol concentrations are no longer statistically significant (Figure 2) in a model that accounts for voice volume and CO2 emissions, but the effect of singing (vs talking) persists. Singing produced an estimated 64% (95% CI: 28–114%) more particles on a per-breath (or per-CO2 basis) than talking, while each ∼5 dBA increase in volume produced 50% more particles than the reference level of 68 dbA. Our interpretation of these results is that voice loudness and CO2 emission rates are the causal factors influencing our model results. That is, males (and adults) tend to vocalize at higher volumes and emit more CO2 than females (and children), and these behavioral/physiological factors explain most of the age and sex differences in raw aerosol emissions that are shown in Figure 1.

Figure 2

Figure 2. Modeled change (% difference) in exhaled concentrations when accounting for maneuver type, loudness, age, and sex. Error bars represent 95% confidence intervals. Data for particles from 0.25 to 33 μm in diameter.

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These findings imply that indoor monitoring of ambient CO2 levels should account for age and sex differences (in raw respiratory aerosol emissions) and, thus, provide a relatively robust estimator for aerosol-based infection risk, as suggested by Peng. (18) However, our results also suggest that concurrent monitoring of indoor volume levels is warranted, as the volume effect persisted in a model that accounted for exhaled CO2. Further, control of infection risk must also consider room occupancy levels and whether singing or talking is taking place indoors (or neither), as singing produces increased emissions, even after accounting for voice loudness and exhaled CO2.

Strengths, Limitations, and Future Work

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Our study was conducted on a large sample of participants with a wide range of ages, both sexes, and diverse physiology (e.g., varied body sizes), which allows us to draw conclusions about average population-level emissions that are more generalizable to the public than previous studies. The importance of achieving a larger sample size is emphasized by the fact that our study was able to identify several “outlier” individuals, whose emissions varied drastically from others. For example, the highest emitting singer from our sample produced concentrations that were more than 500% higher than the median value (and over 42 times greater than the lowest emitting singer in our sample, both for raw and exhaled emissions). These results support hypotheses that some individuals within a population may be “superspreaders” of infectious respiratory diseases due to individual variations in physiology, in addition to aspects of virology and behavioral patterns that result in more contacts and transmission for certain people compared to others. (18,28−30) More work is needed to determine whether those individuals who produce higher total respiratory aerosol emissions are also capable of emitting higher pathogenic counts (e.g., viral shedding loads), though evidence suggests that SARS-CoV-2 infection produces increased respiratory aerosol emissions. (31)
We conducted our study in a laboratory environment, wherein participants were asked to perform controlled, predetermined vocal maneuvers on command, rather than measuring emissions in a real-world setting. A major benefit of the controlled experimental design is that we could reduce background (ambient air) particle levels through chamber air filtration, which enabled us to better isolate and measure respiratory aerosols from vocalization. Respiratory aerosol emissions occur at levels below typical ambient air concentrations. Reduction of background is critical for making measurements that allow us to statistically differentiate respiratory aerosol levels across activities or demographic factors. However, controlled designs may lack generalizability to real-world situations, as the controlled protocols may be inherently different or lack variability seen in the real world. We attempted to counter this concern by choosing a talking maneuver that was designed to include a range of sounds and speech patterns representative of standard English-language conversations. (19) Similarly, we chose a song for the singing maneuver that was common and basic.
Our study was limited to ages 12 to 64 years old. Whether the relationship we observed between emissions, voice volume, and exhaled CO2 holds for young children, as well as for older adults, is unknown (though our model results are consistent when stratified to include only minors or only adult age groups; data not shown). Additional research is needed to characterize respiratory aerosol emissions during early childhood development. Similarly, while we measured emissions over a range of voice loudness by asking participants to talk and sing, we did not consider other types of vocal activities like shouting or whispering. Our results indicate that voice loudness is an explanatory factor for differences in emissions from talking to singing, and therefore one would hypothesize that shouting (at a higher volume) or whispering (lower volume) would produce more and less emissions, respectively. However, these activities were not evaluated here.
We did not quantify respiratory disease transmission risk. For safety purposes, we limited participants to healthy individuals who were not experiencing any symptoms of COVID-19 (or other respiratory illness) and had no known recent exposure to someone who was sick with COVID-19. The amount of respiratory aerosol generated by an individual is but one of several factors that play a role in transmission. Factors such as the pathogen’s infectious dose, viral loads in the source individual, and susceptibility of the host (which may be impacted by individual’s physiology, genetics, and comorbidities), as well as a wide range of environmental and social factors related to human-to-human interactions all impact the likelihood that a disease is transmitted from one individual to another. Our results suggest that measuring volume and exhaled CO2 may be useful proxies for respiratory aerosol emissions indoors. However, further work is needed to understand how these proxies correlate to risk. For example, although people naturally tend to vocalize at a loudness levels above ambient background, it is unclear whether monitoring the loudness of specific vocal frequencies or total noise (i.e., average A-weighted decibels) would be needed. Additionally, while our work suggests that exhaled CO2 and voice volume have potential for understanding average population emissions, neither of these metrics explains the “superemission” phenomenon, which was evident among at least one of our participants. There is large interindividual variation in respiratory aerosol emissions. Future work to validate CO2 and loudness as indicators of infection risk should also investigate, within real-world built environment settings, how nonvocal respiratory emissions (i.e., breathing), nonhuman sources of CO2 (e.g., combustion for cooking, room heating, and cooling) and noise, and aerosol sinks such as in-room filtration interact and influence these metrics across space and time.

Supporting Information

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The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.estlett.1c00760.

  • Details on data handling and statistical analyses and results of histogram of participants by age (Figure S1), description of testing facility and sampling schematic (Figure S2), signal-to-noise ratios for raw concentration data (Figure S3), correlation plots between respiratory aerosol emissions and participant voice volume (Figure S4) and measured CO2 mixing ratios (Figure S5), exhaled respiratory aerosol concentrations (Figure S6), plot of measured aerosol size distribution from singing (Figure S7), and outputs from linear models (Tables S1–S3) (PDF)

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Author Information

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  • Corresponding Author
    • John Volckens - Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, Colorado 80523, United States;  Mechanical Engineering, Colorado State University, Fort Collins, Colorado 80523, United States;  Orcidhttps://orcid.org/0000-0002-7563-9525;  Email: [email protected]
  • Authors
    • Nicholas Good - Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, Colorado 80523, United States
    • Kristen M. Fedak - Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, Colorado 80523, United States
    • Dan Goble - School of Music, Theatre, and Dance, Colorado State University, Fort Collins, Colorado 80523, United States
    • Amy Keisling - School of Music, Theatre, and Dance, Colorado State University, Fort Collins, Colorado 80523, United States;  Mechanical Engineering, Colorado State University, Fort Collins, Colorado 80523, United States
    • Christian L’Orange - Mechanical Engineering, Colorado State University, Fort Collins, Colorado 80523, United States
    • Emily Morton - School of Music, Theatre, and Dance, Colorado State University, Fort Collins, Colorado 80523, United States
    • Rebecca Phillips - School of Music, Theatre, and Dance, Colorado State University, Fort Collins, Colorado 80523, United States
    • Ky Tanner - Mechanical Engineering, Colorado State University, Fort Collins, Colorado 80523, United States
  • Notes
    The authors declare no competing financial interest.

Acknowledgments

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This work was funded by unrestricted philanthropic donations to the School of Music, Theatre, and Dance at Colorado State University. The authors wish to acknowledge input into the experimental design from members of the study scientific advisory board, including Allen Henderson (Georgia Southern University), Charles Henry (Colorado State University), Emily Morgan (Colorado State University), Heather Pidcoke (Colorado State University), and Timothy Rhea (Texas A&M University).

References

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    Exhaled breath condensate (EBC) is increasingly being used as a non-invasive method for disease diagnosis and environmental exposure assessment. By using hydrophobic surface, ice and droplet scavenging, a simple impaction and condensing based collection method is reported here. Human subjects were recruited to exhale toward the device for 1, 2, 3 and 4 min. The exhaled breath quickly formed into tiny droplets on the hydrophobic surface, which were subsequently scavenged into a 10 μL rolling deionized water droplet. The collected EBC was further analyzed using culturing, DNA stain, Scanning Electron Microscope (SEM), polymerase chain reaction (PCR) and colorimetry (VITEK 2) for bacteria and viruses. Exptl. data revealed that bacteria and viruses in EBC can be rapidly collected using the method developed here, with an obsd. efficiency of 100 μL EBC within 1 min. Culturing, DNA stain, SEM and qPCR methods all detected high bacterial concns. up to 7000 CFU/m3 in exhaled breath, including both viable and dead cells of various types. Sphingomonas paucimobilis and Kocuria variants were found dominant in EBC samples using VITEK 2 system. SEM images revealed that most bacteria in exhaled breath are detected in the size range of 0.5-1.0 μm which is able to enable them to remain airborne for a longer time, thus presenting a risk for airborne transmission of potential diseases. Using qPCR, influenza A H3N2 viruses were also detected in one EBC sample. Different from other devices restricted solely to condensation, the developed method can be easily achieved both by impaction and condensation in a lab. and could impact current practice of EBC collection. Nonetheless, the reported work is a proof-of-concept demonstration and its performance in non-invasive disease diagnosis such as bacteremia and virus infections needs to be further validated including effects of its influencing matrix.
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  4. 4
    Ryan, D. J.; Toomey, S.; Madden, S. F.; Casey, M.; Breathnach, O. S.; Morris, P. G.; Grogan, L.; Branagan, P.; Costello, R. W.; De Barra, E. Use of exhaled breath condensate (EBC) in the diagnosis of SARS-COV-2 (COVID-19). Thorax 2021, 76 (1), 86– 88,  DOI: 10.1136/thoraxjnl-2020-215705
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    Use of exhaled breath condensate (EBC) in the diagnosis of SARS-COV-2 (COVID-19)
    Ryan Daniel J; Toomey Sinead; Hennessy Bryan T; Ryan Daniel J; Casey Michelle; Branagan Peter; Costello Richard W; Hurley Killian; Gunaratnam Cedric; McElvaney Noel G; OBrien Michael Emmet; Sulaiman Imran; Morgan Ross K; Madden Stephen F; Breathnach Oscar S; Morris Patrick G; Grogan Liam; Hennessy Bryan T; De Barra Eoghan
    Thorax (2021), 76 (1), 86-88 ISSN:.
    False negatives from nasopharyngeal swabs (NPS) using reverse transcriptase PCR (RT-PCR) in SARS-CoV-2 are high. Exhaled breath condensate (EBC) contains lower respiratory droplets that may improve detection. We performed EBC RT-PCR for SARS-CoV-2 genes (E, S, N, ORF1ab) on NPS-positive (n=16) and NPS-negative/clinically positive COVID-19 patients (n=15) using two commercial assays. EBC detected SARS-CoV-2 in 93.5% (29/31) using the four genes. Pre-SARS-CoV-2 era controls (n=14) were negative. EBC was positive in NPS negative/clinically positive patients in 66.6% (10/15) using the identical E and S (E/S) gene assay used for NPS, 73.3% (11/15) using the N/ORF1ab assay and 14/15 (93.3%) combined.
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  5. 5
    Patterson, B.; Bryden, W.; Call, C.; McKerry, A.; Leonard, B.; Seldon, R.; Gqada, M.; Dinkele, R.; Gessner, S.; Warner, D. F. Cough-independent production of viable Mycobacterium tuberculosis in bioaerosol. Tuberculosis 2021, 126, 102038,  DOI: 10.1016/j.tube.2020.102038
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    Cough-independent production of viable Mycobacterium tuberculosis in bioaerosol
    Patterson, Benjamin; Bryden, Wayne; Call, Charles; McKerry, Andrea; Leonard, Bryan; Seldon, Ronnett; Gqada, Melitta; Dinkele, Ryan; Gessner, Sophia; Warner, Digby F.; Wood, Robin
    Tuberculosis (Oxford, United Kingdom) (2021), 126 (), 102038CODEN: TUBECU; ISSN:1472-9792. (Elsevier Ltd.)
    Symptoms of infectious respiratory illnesses are often assumed to drive transmission. However, prodn. and release of Mycobacterium tuberculosis (Mtb) bioaerosols is poorly understood. We report quantitation of Mtb exhaled during specific respiratory manoeuvres. Direct capture of nascent bioaerosol particles and indirect collection of aged particles was performed in 10 healthy subjects. Indirect and direct capture of exhaled viable Mtb bacilli was compared in 38 PTB patients and directly captured viable Mtb during cough and bronchiole-burst manoeuvres in 27 of the PTB patients. Direct sampling of healthy subjects captured larger bioaerosol vols. with higher proportions of 2-5μm particles than indirect sampling. Indirect sampling identified viable Mtb in 92.1% (35 of 38) of PTB patients during 60-min relaxed breathing, median bacillary count 7.5 (IQR: 3.25-19). Direct sampling for 10-min identified Mtb in 97.4% (37 of 38) of PTB patients with higher bacilli counts (p < 0.001), median 24.5 (IQR:11.25-37.5). A short 5-min sampling regimen of 10 coughs or 10 bronchiole-burst manoeuvres yielded a median of 11 (IQR: 4-17) and 11 (IQR: 7-17.5) Mtb bacilli, resp. (p = 0.53). Peripheral lung bioaerosol released through deep exhalations alone contained viable Mtb suggesting non-cough transmission is possible in PTB.
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    Morawska, L.; Cao, J. Airborne transmission of SARS-CoV-2: The world should face the reality. Environ. Int. 2020, 139, 105730,  DOI: 10.1016/j.envint.2020.105730
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    Airborne transmission of SARS-CoV-2: The world should face the reality
    Morawska, Lidia; Cao, Junji
    Environment International (2020), 139 (), 105730CODEN: ENVIDV; ISSN:0160-4120. (Elsevier Ltd.)
    Hand washing and maintaining social distance are the main measures recommended by the World Health Organization (WHO) to avoid contracting COVID-19. Unfortunately, these measured do not prevent infection by inhalation of small droplets exhaled by an infected person that can travel distance of meters or tens of meters in the air and carry their viral content. Science explains the mechanisms of such transport and there is evidence that this is a significant route of infection in indoor environments. Despite this, no countries or authorities consider airborne spread of COVID-19 in their regulations to prevent infections transmission indoors. It is therefore extremely important, that the national authorities acknowledge the reality that the virus spreads through air, and recommend that adequate control measures be implemented to prevent further spread of the SARS-CoV-2 virus, in particularly removal of the virus-laden droplets from indoor air by ventilation.
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    Setti, L.; Passarini, F.; De Gennaro, G.; Barbieri, P.; Perrone, M. G.; Borelli, M.; Palmisani, J.; Di Gilio, A.; Piscitelli, P.; Miani, A. Airborne transmission route of COVID-19: why 2 meters/6 feet of inter-personal distance could not be enough. Int. J. Environ. Res. Public Health 2020, 17, 2932,  DOI: 10.3390/ijerph17082932
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    Airborne transmission route of COVID-19: why 2 meters/6 feet of inter-personal distance could not be enough
    Setti, Leonardo; Passarini, Fabrizio; De Gennaro, Gianluigi; Barbieri, Pierluigi; Perrone, Maria Grazia; Borelli, Massimo; Palmisani, Jolanda; Di Gilio, Alessia; Piscitelli, Prisco; Miani, Alessandro
    International Journal of Environmental Research and Public Health (2020), 17 (8), 2932CODEN: IJERGQ; ISSN:1660-4601. (MDPI AG)
    The COVID-19 pandemic caused the shutdown of entire nations all over the world. In addn. to mobility restrictions of people, the World Health Organization and the Governments have prescribed maintaining an inter-personal distance of 1.5 or 2 m (∼6 ft) from each other to minimize the risk of contagion through the droplets that we usually disseminate around us from nose and mouth. However, recently published studies support the hypothesis of virus transmission over a distance of 2 m from an infected person. Researchers have proved the higher aerosol and surface stability of SARS-COV-2 as compared with SARS-COV-1 (with the virus remaining viable and infectious in aerosol for hours) and that airborne transmission of SARS-CoV can occur besides close-distance contacts. Indeed, there is reasonable evidence about the possibility of SARS-COV-2 airborne transmission due to its persistence into aerosol droplets in a viable and infectious form. Based on the available knowledge and epidemiol. observations, it is plausible that small particles contg. the virus may diffuse in indoor environments covering distances ≤10 m from the emission sources, thus representing a kind of aerosol transmission. On-field studies carried out inside Wuhan Hospitals showed the presence of SARS-COV-2 RNA in air samples collected in the hospitals and also in the surroundings, leading to the conclusion that the airborne route has to be considered an important pathway for viral diffusion. Similar findings are reported in analyses concerning air samples collected at the Nebraska University Hospital. On March 16th, we have released a Position Paper emphasizing the airborne route as a possible addnl. factor for interpreting the anomalous COVID-19 outbreaks in northern Italy, ranked as 1 of the most polluted areas in Europe and characterized by high particulate matter (PM) concns. The available information on the SARS-COV-2 spreading supports the hypothesis of airborne diffusion of infected droplets from person to person at a distance >2 m (6 ft). The inter-personal distance of 2 m can be reasonably considered as an effective protection only if everybody wears face masks in daily life activities.
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    Azimi, P.; Keshavarz, Z.; Laurent, J. G. C.; Stephens, B.; Allen, J. G. Mechanistic transmission modeling of COVID-19 on the Diamond Princess cruise ship demonstrates the importance of aerosol transmission. Proc. Natl. Acad. Sci. U. S. A. 2021, 118 (8), e2015482118,  DOI: 10.1073/pnas.2015482118
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    Mechanistic transmission modeling of COVID-19 on the Diamond Princess cruise ship demonstrates the importance of aerosol transmission
    Azimi, Parham; Keshavarz, Zahra; Cedeno Laurent, Jose Guillermo; Stephens, Brent; Allen, Joseph G.
    Proceedings of the National Academy of Sciences of the United States of America (2021), 118 (8), e2015482118CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
    Several lines of existing evidence support the possibility of airborne transmission of coronavirus disease 2019 (COVID-19). However, quant. information on the relative importance of transmission pathways of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) remains limited. To evaluate the relative importance of multiple transmission routes for SARS-CoV-2, we developed a modeling framework and leveraged detailed information available from the Diamond Princess cruise ship outbreak that occurred in early 2020. We modeled 21,600 scenarios to generate a matrix of solns. across a full range of assumptions for eight unknown or uncertain epidemic and mechanistic transmission factors. A total of 132 model iterations met acceptability criteria (R2 > 0.95 for modeled vs. reported cumulative daily cases and R2 > 0 for daily cases). Analyzing only these successful model iterations quantifies the likely contributions of each defined mode of transmission. Mean ests. of the contributions of short-range, long-range, and fomite transmission modes to infected cases across the entire simulation period were 35%, 35%, and 30%, resp. Mean ests. of the contributions of larger respiratory droplets and smaller respiratory aerosols were 41% and 59%, resp. Our results demonstrate that aerosol inhalation was likely the dominant contributor to COVID-19 transmission among the passengers, even considering a conservative assumption of high ventilation rates and no air recirculation conditions for the cruise ship. Moreover, close-range and long-range transmission likely contributed similarly to disease progression aboard the ship, with fomite transmission playing a smaller role. The passenger quarantine also affected the importance of each mode, demonstrating the impacts of the interventions.
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    Nazaroff, W. W. Indoor bioaerosol dynamics. Indoor Air 2016, 26 (1), 61– 78,  DOI: 10.1111/ina.12174
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    Indoor bioaerosol dynamics
    Nazaroff, William W.
    Indoor Air (2016), 26 (1), 61-78CODEN: INAIE5; ISSN:1600-0668. (Wiley-Blackwell)
    Inhaling indoor air is the primary means by which humans are exposed to bioaerosols. Considering bacteria, fungi, and viruses, this study reviews the dynamic processes that govern indoor concns. and fates of biol. particulate material. Bioaerosol behavior is strongly coupled to particle size; this study emphasizes the range 0.1-10 μm in aerodynamic diam. The principle of material balance allows concns. to be detd. from knowledge of important source and removal processes. Sources reviewed here include outdoor air introduced by air exchange plus indoor emission from occupants, occupant activities, and moldy materials. Important mechanisms that remove bioaerosols from indoor air include air exchange, deposition onto indoor surfaces, and active filtration. The review summarizes knowledge about size-dependent particle deposition in different regions of the respiratory tract, techniques for measuring indoor bioaerosols, and evidence for diseases caused by airborne exposure to bioaerosols. Future research challenges and opportunities are highlighted.
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    Kriebel, D.; Tickner, J.; Epstein, P.; Lemons, J.; Levins, R.; Loechler, E. L.; Quinn, M.; Rudel, R.; Schettler, T.; Stoto, M. The precautionary principle in environmental science. Environ. Health Perspect. 2001, 109 (9), 871– 876,  DOI: 10.1289/ehp.01109871
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    The precautionary principle in environmental science
    Kriebel D; Tickner J; Epstein P; Lemons J; Levins R; Loechler E L; Quinn M; Rudel R; Schettler T; Stoto M
    Environmental health perspectives (2001), 109 (9), 871-6 ISSN:0091-6765.
    Environmental scientists play a key role in society's responses to environmental problems, and many of the studies they perform are intended ultimately to affect policy. The precautionary principle, proposed as a new guideline in environmental decision making, has four central components: taking preventive action in the face of uncertainty; shifting the burden of proof to the proponents of an activity; exploring a wide range of alternatives to possibly harmful actions; and increasing public participation in decision making. In this paper we examine the implications of the precautionary principle for environmental scientists, whose work often involves studying highly complex, poorly understood systems, while at the same time facing conflicting pressures from those who seek to balance economic growth and environmental protection. In this complicated and contested terrain, it is useful to examine the methodologies of science and to consider ways that, without compromising integrity and objectivity, research can be more or less helpful to those who would act with precaution. We argue that a shift to more precautionary policies creates opportunities and challenges for scientists to think differently about the ways they conduct studies and communicate results. There is a complicated feedback relation between the discoveries of science and the setting of policy. While maintaining their objectivity and focus on understanding the world, environmental scientists should be aware of the policy uses of their work and of their social responsibility to do science that protects human health and the environment. The precautionary principle highlights this tight, challenging linkage between science and policy.
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    Hamner, L. High SARS-CoV-2 attack rate following exposure at a choir practice─Skagit County, Washington, March 2020. Morb. Mortal. Wkly. Rep. 2020, 69, 606,  DOI: 10.15585/mmwr.mm6919e6
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    11
    High SARS-CoV-2 attack rate following exposure at a choir practice - Skagit County, Washington
    Hamner, Lea; Dubbel, Polly; Capron, Ian; Ross, Andy; Jordan, Amber; Lee, Jaxon; Lynn, Joanne; Ball, Amelia; Narwal, Simranjit; Russell, Sam; Patrick, Dale; Leibrand, Howard
    Morbidity and Mortality Weekly Report (2020), 69 (19), 606-610CODEN: MMWRC7; ISSN:1545-861X. (Centers for Disease Control and Prevention)
    What is already known about this topic. Superspreading events involving SARS-CoV-2, the virus that causes COVID-19, have been reported. What is added by this report. Following a 2.5-h choir practice attended by 61 persons, including a symptomatic index patient, 32 confirmed and 20 probable secondary COVID-19 cases occurred (attack rate = 53.3% to 86.7%); three patients were hospitalized, and two died. Transmission was likely facilitated by close proximity (within 6 ft) during practice and augmented by the act of singing. What are the implications for public health practice. The potential for superspreader events underscores the importance of phys. distancing, including avoiding gathering in large groups, to control spread of COVID-19. Enhancing community awareness can encourage symptomatic persons and contacts of ill persons to isolate or self-quarantine to prevent ongoing transmission.
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    Alsved, M.; Matamis, A.; Bohlin, R.; Richter, M.; Bengtsson, P.-E.; Fraenkel, C.-J.; Medstrand, P.; Löndahl, J. Exhaled respiratory particles during singing and talking. Aerosol Sci. Technol. 2020, 54 (11), 1245– 1248,  DOI: 10.1080/02786826.2020.1812502
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    12
    Exhaled respiratory particles during singing and talking
    Alsved, M.; Matamis, A.; Bohlin, R.; Richter, M.; Bengtsson, P.-E.; Fraenkel, C.-J.; Medstrand, P.; Loendahl, J.
    Aerosol Science and Technology (2020), 54 (11), 1245-1248CODEN: ASTYDQ; ISSN:0278-6826. (Taylor & Francis, Inc.)
    Exhaled respiratory particles during singing and talking.
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    Asadi, S.; Wexler, A. S.; Cappa, C. D.; Barreda, S.; Bouvier, N. M.; Ristenpart, W. D. Effect of voicing and articulation manner on aerosol particle emission during human speech. PLoS One 2020, 15 (1), e0227699,  DOI: 10.1371/journal.pone.0227699
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    13
    Effect of voicing and articulation manner on aerosol particle emission during human speech
    Asadi, Sima; Wexler, Anthony S.; Cappa, Christopher D.; Barreda, Santiago; Bouvier, Nicole M.; Ristenpart, William D.
    PLoS One (2020), 15 (1), e0227699CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
    Previously, we demonstrated a strong correlation between the amplitude of human speech and the emission rate of micron-scale expiratory aerosol particles, which are believed to play a role in respiratory disease transmission. To further those findings, here we systematically investigate the effect of different 'phones' (the basic sound units of speech) on the emission of particles from the human respiratory tract during speech. We measured the respiratory particle emission rates of 56 healthy human volunteers voicing specific phones, both in isolation and in the context of a std. spoken text. Our measurements showed that particle emission rates were pos. correlated with the vowel content of a phrase; conversely, particle emission decreased during phrases with a high fraction of voiceless fricatives. Our particle emission data is broadly consistent with prior measurements of the egressive airflow rate assocd. with the vocalization of various phones that differ in voicing and articulation. These results suggest that airborne transmission of respiratory pathogens via speech aerosol particles could be modulated by specific phonetic characteristics of the language spoken by a given human population, along with other, more frequently considered epidemiol. variables.
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    Mürbe, D.; Kriegel, M.; Lange, J.; Schumann, L.; Hartmann, A.; Fleischer, M. Aerosol emission of adolescents voices during speaking, singing and shouting. PLoS One 2021, 16 (2), e0246819,  DOI: 10.1371/journal.pone.0246819
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    14
    Aerosol emission of adolescents voices during speaking, singing and shouting
    Muerbe, Dirk; Kriegel, Martin; Lange, Julia; Schumann, Lukas; Hartmann, Anne; Fleischer, Mario
    PLoS One (2021), 16 (2), e0246819CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
    Since the outbreak of the COVID-19 pandemic, singing activities for children and young people have been strictly regulated with far-reaching consequences for music education in schools and ensemble and choir singing in some places. This is also due to the fact, that there has been no reliable data available on aerosol emissions from adolescents speaking, singing, and shouting. By utilizing a laser particle counter in clean room conditions we show, that adolescents emit fewer aerosol particles during singing than what has been known so far for adults. In our data, the emission rates ranged from 16 P/s to 267 P/s for speaking, 141 P/s to 1240 P/s for singing, and 683 P/s to 4332 P/s for shouting. The data advocate an adaptation of existing risk management strategies and rules of conduct for groups of singing adolescents, like gatherings in an educational context, e.g. singing lessons or choir rehearsals.
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  15. 15
    Gregson, F. K.; Watson, N. A.; Orton, C. M.; Haddrell, A. E.; McCarthy, L. P.; Finnie, T. J.; Gent, N.; Donaldson, G. C.; Shah, P. L.; Calder, J. D. Comparing aerosol concentrations and particle size distributions generated by singing, speaking and breathing. Aerosol Sci. Technol. 2021, 55 (6), 681– 691,  DOI: 10.1080/02786826.2021.1883544
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    15
    Comparing aerosol concentrations and particle size distributions generated by singing, speaking and breathing
    Gregson, Florence K. A.; Watson, Natalie A.; Orton, Christopher M.; Haddrell, Allen E.; McCarthy, Lauren P.; Finnie, Thomas J. R.; Gent, Nick; Donaldson, Gavin. C.; Shah, Pallav L.; Calder, James D.; Bzdek, Bryan R.; Costello, Declan; Reid, Jonathan P.
    Aerosol Science and Technology (2021), 55 (6), 681-691CODEN: ASTYDQ; ISSN:0278-6826. (Taylor & Francis, Inc.)
    The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic has resulted in an unprecedented shutdown in social and economic activity, with the cultural sector particularly severely affected. Restrictions on musical performances have arisen from a perception that there is a significantly higher risk of aerosol prodn. from singing than speaking, based upon high-profile examples of clusters of COVID-19 following choral rehearsals. However, comparing aerosol generation from different types of vocalization, including singing, across a range of vols. is a rapidly evolving area of research. Here, we measured aerosols from singing, speaking and breathing from a large cohort of 25 professional singers in a range of musical genres in a zero-background environment, allowing unequivocal attribution of aerosol prodn. to specific vocalizations. We do not assess the relative vols. at which people speak and sing. However, both showed steep increases in mass concn. with increase in loudness (spanning a factor of 20-30 across the dynamic range measured, p < 0.001). At the quietest vol. (50 to 60 dBA), neither singing (p = 0.19) nor speaking (p = 0.20) were significantly different to breathing. At the loudest vol. (90 to 100 dBA), a statistically significant difference (p < 0.001) was obsd. between singing and speaking, but with singing only generating a factor of between 1.5 and 3.4 more aerosol mass. Guidelines for musical performances should be based on the loudness and duration of the vocalization, the no. of participants and the environment in which the activity occurs, rather than the type of vocalization. Mitigations such as the use of amplification and increased attention to ventilation should be employed where practicable. Copyright 2021 American Assocn. for Aerosol Research.
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    Asadi, S.; Wexler, A. S.; Cappa, C. D.; Barreda, S.; Bouvier, N. M.; Ristenpart, W. D. Aerosol emission and superemission during human speech increase with voice loudness. Sci. Rep. 2019, 9 (1), 2348,  DOI: 10.1038/s41598-019-38808-z
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    16
    Aerosol emission and superemission during human speech increase with voice loudness
    Asadi Sima; Ristenpart William D; Wexler Anthony S; Wexler Anthony S; Wexler Anthony S; Cappa Christopher D; Wexler Anthony S; Barreda Santiago; Bouvier Nicole M; Bouvier Nicole M
    Scientific reports (2019), 9 (1), 2348 ISSN:.
    Mechanistic hypotheses about airborne infectious disease transmission have traditionally emphasized the role of coughing and sneezing, which are dramatic expiratory events that yield both easily visible droplets and large quantities of particles too small to see by eye. Nonetheless, it has long been known that normal speech also yields large quantities of particles that are too small to see by eye, but are large enough to carry a variety of communicable respiratory pathogens. Here we show that the rate of particle emission during normal human speech is positively correlated with the loudness (amplitude) of vocalization, ranging from approximately 1 to 50 particles per second (0.06 to 3 particles per cm(3)) for low to high amplitudes, regardless of the language spoken (English, Spanish, Mandarin, or Arabic). Furthermore, a small fraction of individuals behaves as "speech superemitters," consistently releasing an order of magnitude more particles than their peers. Our data demonstrate that the phenomenon of speech superemission cannot be fully explained either by the phonic structures or the amplitude of the speech. These results suggest that other unknown physiological factors, varying dramatically among individuals, could affect the probability of respiratory infectious disease transmission, and also help explain the existence of superspreaders who are disproportionately responsible for outbreaks of airborne infectious disease.
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    Mürbe, D.; Kriegel, M.; Lange, J.; Rotheudt, H.; Fleischer, M. Aerosol emission in professional singing of classical music. Sci. Rep. 2021, 11 (1), 14861,  DOI: 10.1038/s41598-021-93281-x
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    17
    Aerosol emission in professional singing of classical music
    Muerbe, Dirk; Kriegel, Martin; Lange, Julia; Rotheudt, Hansjoerg; Fleischer, Mario
    Scientific Reports (2021), 11 (1), 14861CODEN: SRCEC3; ISSN:2045-2322. (Nature Research)
    Abstr.: In this study, emission rates of aerosols emitted by professional singers were measured with a laser particle counter under cleanroom conditions. The emission rates during singing varied between 753 and 6093 particles/s with a median of 1537 particles/s. Emission rates for singing were compared with data for breathing and speaking. Significantly higher emission rates were found for singing. The emission enhancements between singing and speaking were between 4.0 and 99.5 with a median of 17.4, largely due to higher sound pressure levels when singing. Further, significant effects of vocal loudness were found, whereas there were no significant differences between the investigated voice classifications. The present study supports the efforts to improve the risk management in cases of possible aerogenic virus transmission, esp. for choir singing.
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  • Abstract

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    Figure 1

    Figure 1. Raw respiratory aerosol concentrations (0.25–33 μm in diameter) measured across different populations and activities. Solid line represents the median, boxes delineate the IQR, and whiskers represent IQR·1.5 or the data minima. The horizontal, dashed line represents a method quantification limit of 50 particles·L–1. Participant data are shown as open circles.

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    Figure 2

    Figure 2. Modeled change (% difference) in exhaled concentrations when accounting for maneuver type, loudness, age, and sex. Error bars represent 95% confidence intervals. Data for particles from 0.25 to 33 μm in diameter.

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  • References

    This article references 31 other publications.

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      2
      Viable Influenza A Virus in Airborne Particles from Human Coughs
      Lindsley, William G.; Noti, John D.; Blachere, Francoise M.; Thewlis, Robert E.; Martin, Stephen B.; Othumpangat, Sreekumar; Noorbakhsh, Bahar; Goldsmith, William T.; Vishnu, Abhishek; Palmer, Jan E.; Clark, Karen E.; Beezhold, Donald H.
      Journal of Occupational and Environmental Hygiene (2015), 12 (2), 107-113CODEN: JOEHA2; ISSN:1545-9624. (Taylor & Francis, Inc.)
      Patients with influenza release aerosol particles contg. the virus into their environment. However, the importance of airborne transmission in the spread of influenza is unclear, in part because of a lack of information about the infectivity of the airborne virus. The purpose of this study was to det. the amt. of viable influenza A virus that was expelled by patients in aerosol particles while coughing. Sixty-four symptomatic adult volunteer outpatients were asked to cough 6 times into a cough aerosol collection system. Seventeen of these participants tested pos. for influenza A virus by viral plaque assay (VPA) with confirmation by viral replication assay (VRA). Viable influenza A virus was detected in the cough aerosol particles from 7 of these 17 test subjects (41%). Viable influenza A virus was found in the smallest particle size fraction (0.3 μm to 8 μm), with a mean of 142 plaque-forming units (SD 215) expelled during the 6 coughs in particles of this size. These results suggest that a significant proportion of patients with influenza A release small airborne particles contg. viable virus into the environment. Although the amts. of influenza A detected in cough aerosol particles during our expts. were relatively low, larger quantities could be expelled by influenza patients during a pandemic when illnesses would be more severe. Our findings support the idea that airborne infectious particles could play an important role in the spread of influenza.
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    3. 3
      Xu, Z.; Shen, F.; Li, X.; Wu, Y.; Chen, Q.; Jie, X.; Yao, M. Molecular and microscopic analysis of bacteria and viruses in exhaled breath collected using a simple impaction and condensing method. PLoS One 2012, 7 (7), e41137,  DOI: 10.1371/journal.pone.0041137
      3
      Molecular and microscopic analysis of bacteria and viruses in exhaled breath collected using a simple impaction and condensing method
      Xu, Zhenqiang; Shen, Fangxia; Li, Xiaoguang; Wu, Yan; Chen, Qi; Jie, Xu; Yao, Maosheng
      PLoS One (2012), 7 (7), e41137CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
      Exhaled breath condensate (EBC) is increasingly being used as a non-invasive method for disease diagnosis and environmental exposure assessment. By using hydrophobic surface, ice and droplet scavenging, a simple impaction and condensing based collection method is reported here. Human subjects were recruited to exhale toward the device for 1, 2, 3 and 4 min. The exhaled breath quickly formed into tiny droplets on the hydrophobic surface, which were subsequently scavenged into a 10 μL rolling deionized water droplet. The collected EBC was further analyzed using culturing, DNA stain, Scanning Electron Microscope (SEM), polymerase chain reaction (PCR) and colorimetry (VITEK 2) for bacteria and viruses. Exptl. data revealed that bacteria and viruses in EBC can be rapidly collected using the method developed here, with an obsd. efficiency of 100 μL EBC within 1 min. Culturing, DNA stain, SEM and qPCR methods all detected high bacterial concns. up to 7000 CFU/m3 in exhaled breath, including both viable and dead cells of various types. Sphingomonas paucimobilis and Kocuria variants were found dominant in EBC samples using VITEK 2 system. SEM images revealed that most bacteria in exhaled breath are detected in the size range of 0.5-1.0 μm which is able to enable them to remain airborne for a longer time, thus presenting a risk for airborne transmission of potential diseases. Using qPCR, influenza A H3N2 viruses were also detected in one EBC sample. Different from other devices restricted solely to condensation, the developed method can be easily achieved both by impaction and condensation in a lab. and could impact current practice of EBC collection. Nonetheless, the reported work is a proof-of-concept demonstration and its performance in non-invasive disease diagnosis such as bacteremia and virus infections needs to be further validated including effects of its influencing matrix.
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    4. 4
      Ryan, D. J.; Toomey, S.; Madden, S. F.; Casey, M.; Breathnach, O. S.; Morris, P. G.; Grogan, L.; Branagan, P.; Costello, R. W.; De Barra, E. Use of exhaled breath condensate (EBC) in the diagnosis of SARS-COV-2 (COVID-19). Thorax 2021, 76 (1), 86– 88,  DOI: 10.1136/thoraxjnl-2020-215705
      4
      Use of exhaled breath condensate (EBC) in the diagnosis of SARS-COV-2 (COVID-19)
      Ryan Daniel J; Toomey Sinead; Hennessy Bryan T; Ryan Daniel J; Casey Michelle; Branagan Peter; Costello Richard W; Hurley Killian; Gunaratnam Cedric; McElvaney Noel G; OBrien Michael Emmet; Sulaiman Imran; Morgan Ross K; Madden Stephen F; Breathnach Oscar S; Morris Patrick G; Grogan Liam; Hennessy Bryan T; De Barra Eoghan
      Thorax (2021), 76 (1), 86-88 ISSN:.
      False negatives from nasopharyngeal swabs (NPS) using reverse transcriptase PCR (RT-PCR) in SARS-CoV-2 are high. Exhaled breath condensate (EBC) contains lower respiratory droplets that may improve detection. We performed EBC RT-PCR for SARS-CoV-2 genes (E, S, N, ORF1ab) on NPS-positive (n=16) and NPS-negative/clinically positive COVID-19 patients (n=15) using two commercial assays. EBC detected SARS-CoV-2 in 93.5% (29/31) using the four genes. Pre-SARS-CoV-2 era controls (n=14) were negative. EBC was positive in NPS negative/clinically positive patients in 66.6% (10/15) using the identical E and S (E/S) gene assay used for NPS, 73.3% (11/15) using the N/ORF1ab assay and 14/15 (93.3%) combined.
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    5. 5
      Patterson, B.; Bryden, W.; Call, C.; McKerry, A.; Leonard, B.; Seldon, R.; Gqada, M.; Dinkele, R.; Gessner, S.; Warner, D. F. Cough-independent production of viable Mycobacterium tuberculosis in bioaerosol. Tuberculosis 2021, 126, 102038,  DOI: 10.1016/j.tube.2020.102038
      5
      Cough-independent production of viable Mycobacterium tuberculosis in bioaerosol
      Patterson, Benjamin; Bryden, Wayne; Call, Charles; McKerry, Andrea; Leonard, Bryan; Seldon, Ronnett; Gqada, Melitta; Dinkele, Ryan; Gessner, Sophia; Warner, Digby F.; Wood, Robin
      Tuberculosis (Oxford, United Kingdom) (2021), 126 (), 102038CODEN: TUBECU; ISSN:1472-9792. (Elsevier Ltd.)
      Symptoms of infectious respiratory illnesses are often assumed to drive transmission. However, prodn. and release of Mycobacterium tuberculosis (Mtb) bioaerosols is poorly understood. We report quantitation of Mtb exhaled during specific respiratory manoeuvres. Direct capture of nascent bioaerosol particles and indirect collection of aged particles was performed in 10 healthy subjects. Indirect and direct capture of exhaled viable Mtb bacilli was compared in 38 PTB patients and directly captured viable Mtb during cough and bronchiole-burst manoeuvres in 27 of the PTB patients. Direct sampling of healthy subjects captured larger bioaerosol vols. with higher proportions of 2-5μm particles than indirect sampling. Indirect sampling identified viable Mtb in 92.1% (35 of 38) of PTB patients during 60-min relaxed breathing, median bacillary count 7.5 (IQR: 3.25-19). Direct sampling for 10-min identified Mtb in 97.4% (37 of 38) of PTB patients with higher bacilli counts (p < 0.001), median 24.5 (IQR:11.25-37.5). A short 5-min sampling regimen of 10 coughs or 10 bronchiole-burst manoeuvres yielded a median of 11 (IQR: 4-17) and 11 (IQR: 7-17.5) Mtb bacilli, resp. (p = 0.53). Peripheral lung bioaerosol released through deep exhalations alone contained viable Mtb suggesting non-cough transmission is possible in PTB.
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    6. 6
      Morawska, L.; Cao, J. Airborne transmission of SARS-CoV-2: The world should face the reality. Environ. Int. 2020, 139, 105730,  DOI: 10.1016/j.envint.2020.105730
      6
      Airborne transmission of SARS-CoV-2: The world should face the reality
      Morawska, Lidia; Cao, Junji
      Environment International (2020), 139 (), 105730CODEN: ENVIDV; ISSN:0160-4120. (Elsevier Ltd.)
      Hand washing and maintaining social distance are the main measures recommended by the World Health Organization (WHO) to avoid contracting COVID-19. Unfortunately, these measured do not prevent infection by inhalation of small droplets exhaled by an infected person that can travel distance of meters or tens of meters in the air and carry their viral content. Science explains the mechanisms of such transport and there is evidence that this is a significant route of infection in indoor environments. Despite this, no countries or authorities consider airborne spread of COVID-19 in their regulations to prevent infections transmission indoors. It is therefore extremely important, that the national authorities acknowledge the reality that the virus spreads through air, and recommend that adequate control measures be implemented to prevent further spread of the SARS-CoV-2 virus, in particularly removal of the virus-laden droplets from indoor air by ventilation.
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    7. 7
      Setti, L.; Passarini, F.; De Gennaro, G.; Barbieri, P.; Perrone, M. G.; Borelli, M.; Palmisani, J.; Di Gilio, A.; Piscitelli, P.; Miani, A. Airborne transmission route of COVID-19: why 2 meters/6 feet of inter-personal distance could not be enough. Int. J. Environ. Res. Public Health 2020, 17, 2932,  DOI: 10.3390/ijerph17082932
      7
      Airborne transmission route of COVID-19: why 2 meters/6 feet of inter-personal distance could not be enough
      Setti, Leonardo; Passarini, Fabrizio; De Gennaro, Gianluigi; Barbieri, Pierluigi; Perrone, Maria Grazia; Borelli, Massimo; Palmisani, Jolanda; Di Gilio, Alessia; Piscitelli, Prisco; Miani, Alessandro
      International Journal of Environmental Research and Public Health (2020), 17 (8), 2932CODEN: IJERGQ; ISSN:1660-4601. (MDPI AG)
      The COVID-19 pandemic caused the shutdown of entire nations all over the world. In addn. to mobility restrictions of people, the World Health Organization and the Governments have prescribed maintaining an inter-personal distance of 1.5 or 2 m (∼6 ft) from each other to minimize the risk of contagion through the droplets that we usually disseminate around us from nose and mouth. However, recently published studies support the hypothesis of virus transmission over a distance of 2 m from an infected person. Researchers have proved the higher aerosol and surface stability of SARS-COV-2 as compared with SARS-COV-1 (with the virus remaining viable and infectious in aerosol for hours) and that airborne transmission of SARS-CoV can occur besides close-distance contacts. Indeed, there is reasonable evidence about the possibility of SARS-COV-2 airborne transmission due to its persistence into aerosol droplets in a viable and infectious form. Based on the available knowledge and epidemiol. observations, it is plausible that small particles contg. the virus may diffuse in indoor environments covering distances ≤10 m from the emission sources, thus representing a kind of aerosol transmission. On-field studies carried out inside Wuhan Hospitals showed the presence of SARS-COV-2 RNA in air samples collected in the hospitals and also in the surroundings, leading to the conclusion that the airborne route has to be considered an important pathway for viral diffusion. Similar findings are reported in analyses concerning air samples collected at the Nebraska University Hospital. On March 16th, we have released a Position Paper emphasizing the airborne route as a possible addnl. factor for interpreting the anomalous COVID-19 outbreaks in northern Italy, ranked as 1 of the most polluted areas in Europe and characterized by high particulate matter (PM) concns. The available information on the SARS-COV-2 spreading supports the hypothesis of airborne diffusion of infected droplets from person to person at a distance >2 m (6 ft). The inter-personal distance of 2 m can be reasonably considered as an effective protection only if everybody wears face masks in daily life activities.
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    8. 8
      Azimi, P.; Keshavarz, Z.; Laurent, J. G. C.; Stephens, B.; Allen, J. G. Mechanistic transmission modeling of COVID-19 on the Diamond Princess cruise ship demonstrates the importance of aerosol transmission. Proc. Natl. Acad. Sci. U. S. A. 2021, 118 (8), e2015482118,  DOI: 10.1073/pnas.2015482118
      8
      Mechanistic transmission modeling of COVID-19 on the Diamond Princess cruise ship demonstrates the importance of aerosol transmission
      Azimi, Parham; Keshavarz, Zahra; Cedeno Laurent, Jose Guillermo; Stephens, Brent; Allen, Joseph G.
      Proceedings of the National Academy of Sciences of the United States of America (2021), 118 (8), e2015482118CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
      Several lines of existing evidence support the possibility of airborne transmission of coronavirus disease 2019 (COVID-19). However, quant. information on the relative importance of transmission pathways of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) remains limited. To evaluate the relative importance of multiple transmission routes for SARS-CoV-2, we developed a modeling framework and leveraged detailed information available from the Diamond Princess cruise ship outbreak that occurred in early 2020. We modeled 21,600 scenarios to generate a matrix of solns. across a full range of assumptions for eight unknown or uncertain epidemic and mechanistic transmission factors. A total of 132 model iterations met acceptability criteria (R2 > 0.95 for modeled vs. reported cumulative daily cases and R2 > 0 for daily cases). Analyzing only these successful model iterations quantifies the likely contributions of each defined mode of transmission. Mean ests. of the contributions of short-range, long-range, and fomite transmission modes to infected cases across the entire simulation period were 35%, 35%, and 30%, resp. Mean ests. of the contributions of larger respiratory droplets and smaller respiratory aerosols were 41% and 59%, resp. Our results demonstrate that aerosol inhalation was likely the dominant contributor to COVID-19 transmission among the passengers, even considering a conservative assumption of high ventilation rates and no air recirculation conditions for the cruise ship. Moreover, close-range and long-range transmission likely contributed similarly to disease progression aboard the ship, with fomite transmission playing a smaller role. The passenger quarantine also affected the importance of each mode, demonstrating the impacts of the interventions.
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    9. 9
      Nazaroff, W. W. Indoor bioaerosol dynamics. Indoor Air 2016, 26 (1), 61– 78,  DOI: 10.1111/ina.12174
      9
      Indoor bioaerosol dynamics
      Nazaroff, William W.
      Indoor Air (2016), 26 (1), 61-78CODEN: INAIE5; ISSN:1600-0668. (Wiley-Blackwell)
      Inhaling indoor air is the primary means by which humans are exposed to bioaerosols. Considering bacteria, fungi, and viruses, this study reviews the dynamic processes that govern indoor concns. and fates of biol. particulate material. Bioaerosol behavior is strongly coupled to particle size; this study emphasizes the range 0.1-10 μm in aerodynamic diam. The principle of material balance allows concns. to be detd. from knowledge of important source and removal processes. Sources reviewed here include outdoor air introduced by air exchange plus indoor emission from occupants, occupant activities, and moldy materials. Important mechanisms that remove bioaerosols from indoor air include air exchange, deposition onto indoor surfaces, and active filtration. The review summarizes knowledge about size-dependent particle deposition in different regions of the respiratory tract, techniques for measuring indoor bioaerosols, and evidence for diseases caused by airborne exposure to bioaerosols. Future research challenges and opportunities are highlighted.
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    10. 10
      Kriebel, D.; Tickner, J.; Epstein, P.; Lemons, J.; Levins, R.; Loechler, E. L.; Quinn, M.; Rudel, R.; Schettler, T.; Stoto, M. The precautionary principle in environmental science. Environ. Health Perspect. 2001, 109 (9), 871– 876,  DOI: 10.1289/ehp.01109871
      10
      The precautionary principle in environmental science
      Kriebel D; Tickner J; Epstein P; Lemons J; Levins R; Loechler E L; Quinn M; Rudel R; Schettler T; Stoto M
      Environmental health perspectives (2001), 109 (9), 871-6 ISSN:0091-6765.
      Environmental scientists play a key role in society's responses to environmental problems, and many of the studies they perform are intended ultimately to affect policy. The precautionary principle, proposed as a new guideline in environmental decision making, has four central components: taking preventive action in the face of uncertainty; shifting the burden of proof to the proponents of an activity; exploring a wide range of alternatives to possibly harmful actions; and increasing public participation in decision making. In this paper we examine the implications of the precautionary principle for environmental scientists, whose work often involves studying highly complex, poorly understood systems, while at the same time facing conflicting pressures from those who seek to balance economic growth and environmental protection. In this complicated and contested terrain, it is useful to examine the methodologies of science and to consider ways that, without compromising integrity and objectivity, research can be more or less helpful to those who would act with precaution. We argue that a shift to more precautionary policies creates opportunities and challenges for scientists to think differently about the ways they conduct studies and communicate results. There is a complicated feedback relation between the discoveries of science and the setting of policy. While maintaining their objectivity and focus on understanding the world, environmental scientists should be aware of the policy uses of their work and of their social responsibility to do science that protects human health and the environment. The precautionary principle highlights this tight, challenging linkage between science and policy.
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    11. 11
      Hamner, L. High SARS-CoV-2 attack rate following exposure at a choir practice─Skagit County, Washington, March 2020. Morb. Mortal. Wkly. Rep. 2020, 69, 606,  DOI: 10.15585/mmwr.mm6919e6
      11
      High SARS-CoV-2 attack rate following exposure at a choir practice - Skagit County, Washington
      Hamner, Lea; Dubbel, Polly; Capron, Ian; Ross, Andy; Jordan, Amber; Lee, Jaxon; Lynn, Joanne; Ball, Amelia; Narwal, Simranjit; Russell, Sam; Patrick, Dale; Leibrand, Howard
      Morbidity and Mortality Weekly Report (2020), 69 (19), 606-610CODEN: MMWRC7; ISSN:1545-861X. (Centers for Disease Control and Prevention)
      What is already known about this topic. Superspreading events involving SARS-CoV-2, the virus that causes COVID-19, have been reported. What is added by this report. Following a 2.5-h choir practice attended by 61 persons, including a symptomatic index patient, 32 confirmed and 20 probable secondary COVID-19 cases occurred (attack rate = 53.3% to 86.7%); three patients were hospitalized, and two died. Transmission was likely facilitated by close proximity (within 6 ft) during practice and augmented by the act of singing. What are the implications for public health practice. The potential for superspreader events underscores the importance of phys. distancing, including avoiding gathering in large groups, to control spread of COVID-19. Enhancing community awareness can encourage symptomatic persons and contacts of ill persons to isolate or self-quarantine to prevent ongoing transmission.
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    12. 12
      Alsved, M.; Matamis, A.; Bohlin, R.; Richter, M.; Bengtsson, P.-E.; Fraenkel, C.-J.; Medstrand, P.; Löndahl, J. Exhaled respiratory particles during singing and talking. Aerosol Sci. Technol. 2020, 54 (11), 1245– 1248,  DOI: 10.1080/02786826.2020.1812502
      12
      Exhaled respiratory particles during singing and talking
      Alsved, M.; Matamis, A.; Bohlin, R.; Richter, M.; Bengtsson, P.-E.; Fraenkel, C.-J.; Medstrand, P.; Loendahl, J.
      Aerosol Science and Technology (2020), 54 (11), 1245-1248CODEN: ASTYDQ; ISSN:0278-6826. (Taylor & Francis, Inc.)
      Exhaled respiratory particles during singing and talking.
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    13. 13
      Asadi, S.; Wexler, A. S.; Cappa, C. D.; Barreda, S.; Bouvier, N. M.; Ristenpart, W. D. Effect of voicing and articulation manner on aerosol particle emission during human speech. PLoS One 2020, 15 (1), e0227699,  DOI: 10.1371/journal.pone.0227699
      13
      Effect of voicing and articulation manner on aerosol particle emission during human speech
      Asadi, Sima; Wexler, Anthony S.; Cappa, Christopher D.; Barreda, Santiago; Bouvier, Nicole M.; Ristenpart, William D.
      PLoS One (2020), 15 (1), e0227699CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
      Previously, we demonstrated a strong correlation between the amplitude of human speech and the emission rate of micron-scale expiratory aerosol particles, which are believed to play a role in respiratory disease transmission. To further those findings, here we systematically investigate the effect of different 'phones' (the basic sound units of speech) on the emission of particles from the human respiratory tract during speech. We measured the respiratory particle emission rates of 56 healthy human volunteers voicing specific phones, both in isolation and in the context of a std. spoken text. Our measurements showed that particle emission rates were pos. correlated with the vowel content of a phrase; conversely, particle emission decreased during phrases with a high fraction of voiceless fricatives. Our particle emission data is broadly consistent with prior measurements of the egressive airflow rate assocd. with the vocalization of various phones that differ in voicing and articulation. These results suggest that airborne transmission of respiratory pathogens via speech aerosol particles could be modulated by specific phonetic characteristics of the language spoken by a given human population, along with other, more frequently considered epidemiol. variables.
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    14. 14
      Mürbe, D.; Kriegel, M.; Lange, J.; Schumann, L.; Hartmann, A.; Fleischer, M. Aerosol emission of adolescents voices during speaking, singing and shouting. PLoS One 2021, 16 (2), e0246819,  DOI: 10.1371/journal.pone.0246819
      14
      Aerosol emission of adolescents voices during speaking, singing and shouting
      Muerbe, Dirk; Kriegel, Martin; Lange, Julia; Schumann, Lukas; Hartmann, Anne; Fleischer, Mario
      PLoS One (2021), 16 (2), e0246819CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
      Since the outbreak of the COVID-19 pandemic, singing activities for children and young people have been strictly regulated with far-reaching consequences for music education in schools and ensemble and choir singing in some places. This is also due to the fact, that there has been no reliable data available on aerosol emissions from adolescents speaking, singing, and shouting. By utilizing a laser particle counter in clean room conditions we show, that adolescents emit fewer aerosol particles during singing than what has been known so far for adults. In our data, the emission rates ranged from 16 P/s to 267 P/s for speaking, 141 P/s to 1240 P/s for singing, and 683 P/s to 4332 P/s for shouting. The data advocate an adaptation of existing risk management strategies and rules of conduct for groups of singing adolescents, like gatherings in an educational context, e.g. singing lessons or choir rehearsals.
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    15. 15
      Gregson, F. K.; Watson, N. A.; Orton, C. M.; Haddrell, A. E.; McCarthy, L. P.; Finnie, T. J.; Gent, N.; Donaldson, G. C.; Shah, P. L.; Calder, J. D. Comparing aerosol concentrations and particle size distributions generated by singing, speaking and breathing. Aerosol Sci. Technol. 2021, 55 (6), 681– 691,  DOI: 10.1080/02786826.2021.1883544
      15
      Comparing aerosol concentrations and particle size distributions generated by singing, speaking and breathing
      Gregson, Florence K. A.; Watson, Natalie A.; Orton, Christopher M.; Haddrell, Allen E.; McCarthy, Lauren P.; Finnie, Thomas J. R.; Gent, Nick; Donaldson, Gavin. C.; Shah, Pallav L.; Calder, James D.; Bzdek, Bryan R.; Costello, Declan; Reid, Jonathan P.
      Aerosol Science and Technology (2021), 55 (6), 681-691CODEN: ASTYDQ; ISSN:0278-6826. (Taylor & Francis, Inc.)
      The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic has resulted in an unprecedented shutdown in social and economic activity, with the cultural sector particularly severely affected. Restrictions on musical performances have arisen from a perception that there is a significantly higher risk of aerosol prodn. from singing than speaking, based upon high-profile examples of clusters of COVID-19 following choral rehearsals. However, comparing aerosol generation from different types of vocalization, including singing, across a range of vols. is a rapidly evolving area of research. Here, we measured aerosols from singing, speaking and breathing from a large cohort of 25 professional singers in a range of musical genres in a zero-background environment, allowing unequivocal attribution of aerosol prodn. to specific vocalizations. We do not assess the relative vols. at which people speak and sing. However, both showed steep increases in mass concn. with increase in loudness (spanning a factor of 20-30 across the dynamic range measured, p < 0.001). At the quietest vol. (50 to 60 dBA), neither singing (p = 0.19) nor speaking (p = 0.20) were significantly different to breathing. At the loudest vol. (90 to 100 dBA), a statistically significant difference (p < 0.001) was obsd. between singing and speaking, but with singing only generating a factor of between 1.5 and 3.4 more aerosol mass. Guidelines for musical performances should be based on the loudness and duration of the vocalization, the no. of participants and the environment in which the activity occurs, rather than the type of vocalization. Mitigations such as the use of amplification and increased attention to ventilation should be employed where practicable. Copyright 2021 American Assocn. for Aerosol Research.
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    16. 16
      Asadi, S.; Wexler, A. S.; Cappa, C. D.; Barreda, S.; Bouvier, N. M.; Ristenpart, W. D. Aerosol emission and superemission during human speech increase with voice loudness. Sci. Rep. 2019, 9 (1), 2348,  DOI: 10.1038/s41598-019-38808-z
      16
      Aerosol emission and superemission during human speech increase with voice loudness
      Asadi Sima; Ristenpart William D; Wexler Anthony S; Wexler Anthony S; Wexler Anthony S; Cappa Christopher D; Wexler Anthony S; Barreda Santiago; Bouvier Nicole M; Bouvier Nicole M
      Scientific reports (2019), 9 (1), 2348 ISSN:.
      Mechanistic hypotheses about airborne infectious disease transmission have traditionally emphasized the role of coughing and sneezing, which are dramatic expiratory events that yield both easily visible droplets and large quantities of particles too small to see by eye. Nonetheless, it has long been known that normal speech also yields large quantities of particles that are too small to see by eye, but are large enough to carry a variety of communicable respiratory pathogens. Here we show that the rate of particle emission during normal human speech is positively correlated with the loudness (amplitude) of vocalization, ranging from approximately 1 to 50 particles per second (0.06 to 3 particles per cm(3)) for low to high amplitudes, regardless of the language spoken (English, Spanish, Mandarin, or Arabic). Furthermore, a small fraction of individuals behaves as "speech superemitters," consistently releasing an order of magnitude more particles than their peers. Our data demonstrate that the phenomenon of speech superemission cannot be fully explained either by the phonic structures or the amplitude of the speech. These results suggest that other unknown physiological factors, varying dramatically among individuals, could affect the probability of respiratory infectious disease transmission, and also help explain the existence of superspreaders who are disproportionately responsible for outbreaks of airborne infectious disease.
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    17. 17
      Mürbe, D.; Kriegel, M.; Lange, J.; Rotheudt, H.; Fleischer, M. Aerosol emission in professional singing of classical music. Sci. Rep. 2021, 11 (1), 14861,  DOI: 10.1038/s41598-021-93281-x
      17
      Aerosol emission in professional singing of classical music
      Muerbe, Dirk; Kriegel, Martin; Lange, Julia; Rotheudt, Hansjoerg; Fleischer, Mario
      Scientific Reports (2021), 11 (1), 14861CODEN: SRCEC3; ISSN:2045-2322. (Nature Research)
      Abstr.: In this study, emission rates of aerosols emitted by professional singers were measured with a laser particle counter under cleanroom conditions. The emission rates during singing varied between 753 and 6093 particles/s with a median of 1537 particles/s. Emission rates for singing were compared with data for breathing and speaking. Significantly higher emission rates were found for singing. The emission enhancements between singing and speaking were between 4.0 and 99.5 with a median of 17.4, largely due to higher sound pressure levels when singing. Further, significant effects of vocal loudness were found, whereas there were no significant differences between the investigated voice classifications. The present study supports the efforts to improve the risk management in cases of possible aerogenic virus transmission, esp. for choir singing.
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    18. 18
      Peng, Z.; Jimenez, J. L. Exhaled CO2 as a COVID-19 infection risk proxy for different indoor environments and activities. Environ. Sci. Technol. Lett. 2021, 8 (5), 392– 397,  DOI: 10.1021/acs.estlett.1c00183
      18
      Exhaled CO2 as a COVID-19 Infection Risk Proxy for Different Indoor Environments and Activities
      Peng, Zhe; Jimenez, Jose L.
      Environmental Science & Technology Letters (2021), 8 (5), 392-397CODEN: ESTLCU; ISSN:2328-8930. (American Chemical Society)
      CO2 is co-exhaled with aerosols contg. SARS-CoV-2 by COVID-19-infected people and can be used as a proxy of SARS-CoV-2 concns. indoors. Indoor CO2 measurements by low-cost sensors hold promise for mass monitoring of indoor aerosol transmission risk for COVID-19 and other respiratory diseases. We derive anal. expressions of CO2-based risk proxies and apply them to various typical indoor environments. The relative infection risk in a given environment scales with excess CO2 level, and thus, keeping CO2 as low as feasible in a space allows optimization of the protection provided by ventilation. The CO2 level corresponding to a given abs. infection risk varies by >2 orders of magnitude for different environments and activities. Although large uncertainties, mainly from virus exhalation rates, are still assocd. with infection risk ests., our study provides more specific and practical recommendations for low-cost CO2-based indoor infection risk monitoring.
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    19. 19
      Patel, R.; Connaghan, K.; Franco, D.; Edsall, E.; Forgit, D.; Olsen, L.; Ramage, L.; Tyler, E.; Russell, S. The Caterpillar”: A novel reading passage for assessment of motor speech disorders. Am. J. Speech Lang. Pathol. 2013, 22, 1,  DOI: 10.1044/1058-0360(2012/11-0134)
      19
      "The caterpillar": a novel reading passage for assessment of motor speech disorders
      Patel Rupal; Connaghan Kathryn; Franco Diana; Edsall Erika; Forgit Dory; Olsen Laura; Ramage Lianna; Tyler Emily; Russell Scott
      American journal of speech-language pathology (2013), 22 (1), 1-9 ISSN:.
      PURPOSE: A review of the salient characteristics of motor speech disorders and common assessment protocols revealed the need for a novel reading passage tailored specifically to differentiate between and among the dysarthrias (DYSs) and apraxia of speech (AOS). METHOD: "The Caterpillar" passage was designed to provide a contemporary, easily read, contextual speech sample with specific tasks (e.g., prosodic contrasts, words of increasing length and complexity) targeted to inform the assessment of motor speech disorders. Twenty-two adults, 15 with DYS or AOS and 7 healthy controls (HC), were recorded reading "The Caterpillar" passage to demonstrate its utility in examining motor speech performance. CONCLUSION: Analysis of performance across a subset of segmental and prosodic variables illustrated that "The Caterpillar" passage showed promise for extracting individual profiles of impairment that could augment current assessment protocols and inform treatment planning in motor speech disorders.
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    20. 20
      Fedak, K. M.; Good, N.; Walker, E. S.; Balmes, J.; Brook, R. D.; Clark, M. L.; Cole-Hunter, T.; Devlin, R.; L’Orange, C.; Luckasen, G. Acute changes in lung function following controlled exposure to cookstove air pollution in the subclinical tests of volunteers exposed to smoke (STOVES) study. Inhalation Toxicol. 2020, 32 (3), 115– 123,  DOI: 10.1080/08958378.2020.1751750
      20
      Acute changes in lung function following controlled exposure to cookstove air pollution in the subclinical tests of volunteers exposed to smoke (STOVES) study
      Fedak, Kristen M.; Good, Nicholas; Walker, Ethan S.; Balmes, John; Brook, Robert D.; Clark, Maggie L.; Cole-Hunter, Tom; Devlin, Robert; L'Orange, Christian; Luckasen, Gary; Mehaffy, John; Shelton, Rhiannon; Wilson, Ander; Volckens, John; Peel, Jennifer L.
      Inhalation Toxicology (2020), 32 (3), 115-123CODEN: INHTE5; ISSN:0895-8378. (Taylor & Francis Ltd.)
      We investigated acute responses in lung function following controlled exposures to cookstove air pol.. We recruited 48 healthy adult volunteers to undergo six two-hour treatments: filtered-air control and emissions from five different stoves with fine particulate matter (PM2.5) targets from 10 to 500μg/m3. Spirometry was conducted prior to exposure and immediately, and three and 24 h post-exposure. Mixed-effect models were used to est. differences in post-exposure lung function for stove treatments vs. control. Immediately post-exposure, lung function was lower compared to the control for the three highest PM2.5-level stoves. The largest differences were for the fan rocket stove (target 250μg/m3; forced vital capacity (FVC): -60 mL, 95% confidence interval (95% CI) -135, 15; forced expiratory vol. (FEV1): -51 mL, 95% CI -117, 16; mid-expiratory flow (FEF25-75): -116 mL/s, 95% CI -239, 8). At 3 h post-exposure, lung function was lower compared to the control for all stove treatments; effects were of similar magnitude for all stoves. At 24 h post-exposure, results were consistent with a null assocn. for FVC and FEV1; FEF25-75 was lower relative to the control for the gasifier, fan rocket, and three stone fire. Patterns suggesting short-term decreases in lung function follow from exposure to cookstove air pollution even for stove exposures with low PM2.5 levels.
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    21. 21
      Montgomery, D. C.; Peck, E. A.; Vining, G. G. Introduction to linear regression analysis, 6th ed.; John Wiley & Sons: Hoboken, NJ, 2021.
      There is no corresponding record for this reference.
    22. 22
      Johnson, G.; Morawska, L.; Ristovski, Z.; Hargreaves, M.; Mengersen, K.; Chao, C. Y. H.; Wan, M.; Li, Y.; Xie, X.; Katoshevski, D. Modality of human expired aerosol size distributions. J. Aerosol Sci. 2011, 42 (12), 839– 851,  DOI: 10.1016/j.jaerosci.2011.07.009
      22
      Modality of human expired aerosol size distributions
      Johnson, G. R.; Morawska, L.; Ristovski, Z. D.; Hargreaves, M.; Mengersen, K.; Chao, C. Y. H.; Wan, M. P.; Li, Y.; Xie, X.; Katoshevski, D.; Corbett, S.
      Journal of Aerosol Science (2011), 42 (12), 839-851CODEN: JALSB7; ISSN:0021-8502. (Elsevier Ltd.)
      An essential starting point when investigating the potential role of human expired aerosols in the transmission of disease is to gain a comprehensive knowledge of the expired aerosol generation process, including the aerosol size distribution, the various droplet prodn. mechanisms involved and the corresponding sites of prodn. within the respiratory tract. In order to approach this level of understanding we have integrated the results of two different investigative techniques spanning 3 decades of particle size from 700 nm to 1 mm, presenting a single composite size distribution, and identifying the most prominent modes in that distribution. We link these modes to specific sites of origin and mechanisms of prodn. The data for this were obtained using the Aerodynamic Particle Sizer (APS) covering the range 0.7≤d≤20 μm and Droplet Deposition Anal. (DDA) covering the range d≥20 μm. In the case of speech three distinct droplet size distribution modes were identified with count median diams. at 1.6, 2.5 and 145 μm. In the case of voluntary coughing the modes were located at 1.6, 1.7 and 123 μm. The modes are assocd. with three distinct processes: one occurring deep in the lower respiratory tract, another in the region of the larynx and a third in the upper respiratory tract including the oral cavity. The first of these, the Bronchiolar Fluid Film Burst (BFFB or B) mode contains droplets produced during normal breathing. The second, the Laryngeal (L) mode is most active during voicing and coughing. The third, the Oral (O) cavity mode is active during speech and coughing. The no. of droplets and the vol. of aerosol material assocd. with each mode of aerosol prodn. during speech and coughing is presented. The size distribution is modeled as a tri-modal lognormal distribution dubbed the Bronchiolar/Laryngeal/Oral (B.L.O.) tri-modal model.
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    23. 23
      Gramming, P.; Sundberg, J.; Ternström, S.; Leanderson, R.; Perkins, W. H. Relationship between changes in voice pitch and loudness. Journal of voice 1988, 2 (2), 118– 126,  DOI: 10.1016/S0892-1997(88)80067-5
      There is no corresponding record for this reference.
    24. 24
      Dockery, D. W.; Ware, J. H.; Ferris, B. G., Jr; Glicksberg, D. S.; Fay, M. E.; Spiro, A., III; Speizer, F. E. Distribution of forced expiratory volume in one second and forced vital capacity in healthy, white, adult never-smokers in six US cities. Am. Rev. Respir. Dis. 1985, 131 (4), 511– 520,  DOI: 10.1164/arrd.1985.131.4.511
      24
      Distribution of forced expiratory volume in one second and forced vital capacity in healthy, white, adult never-smokers in six U.S. cities
      Dockery D W; Ware J H; Ferris B G Jr; Glicksberg D S; Fay M E; Spiro A 3rd; Speizer F E
      The American review of respiratory disease (1985), 131 (4), 511-20 ISSN:0003-0805.
      As part of a longitudinal study of the respiratory health effects of air pollution, we measured the lung function of 2,454 white adults 25 to 74 yr of age who had never smoked and who reported no respiratory symptoms. These measurements were analyzed to develop a simple model for the cross-sectional dependence of pulmonary function on height, sex, and age. Both forced expiratory volume in one second (FEV1) and forced vital capacity (FVC) can be effectively standardized for body size by dividing each pulmonary function measurement by the square of the standing height (HT2). The age-specific distribution of these standardized measurements is approximately Gaussian, with variance that is independent of age. Plots of FEV1/HT2 and FVC/HT2 against age showed a nonlinear relationship consistent with an increase in the rate of pulmonary function loss with age. On the basis of these graphic analyses, both pulmonary function measurements were fitted to a four-parameter normative model including sex and linear and quadratic terms in age as dependent variables. This model gave predictions that were very close to those from more complicated models currently in use. Predicted percentile levels were calculated for each sex and age, and shown to describe the observations well. The estimated annual change in height-standardized lung function based on the cross-sectional model was compared with the observed change between the first and second examinations of these adults 3 yr later. The observed changes were close to predicted values, except for subjects younger than 35 yr of age at their first examination. The observed change was larger for men than for women. Such simple longitudinal comparisons are subject to selection bias. In this study, subjects in the lowest quartile of FEV1/HT2 for their age and sex at the first examination had a lower probability of providing a lung function measurement 3 yr later.
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    25. 25
      Todisco, T.; Grassi, V.; Dottorini, M.; Sorbini, C. Reference values for flow-volume curves during forced vital capacity breathing in male children and young adults. Respiration 2004, 39 (1), 1– 7,  DOI: 10.1159/000194191
      There is no corresponding record for this reference.
    26. 26
      Holmgren, H.; Ljungström, E. Influence of film dimensions on film droplet formation. J. Aerosol Med. Pulm. Drug Delivery 2012, 25 (1), 47– 53,  DOI: 10.1089/jamp.2011.0892
      26
      Influence of Film Dimensions on Film Droplet Formation
      Holmgren, Helene; Ljungstroem, Evert
      Journal of Aerosol Medicine and Pulmonary Drug Delivery (2012), 25 (1), 47-53CODEN: JAMPC4; ISSN:1941-2711. (Mary Ann Liebert, Inc.)
      Background: Aerosol particles may be generated from rupturing liq. films through a droplet formation mechanism. The present work was undertaken with the aim to throw some light on the influence of film dimensions on droplet formation with possible consequences for exhaled breath aerosol formation.Methods: The film droplet formation process was mimicked by using a purpose-built device, where fluid films were spanned across holes of known diams. As the films burst, droplets were formed and the no. and size distributions of the resulting droplets were detd.Results: No general relation could be found between hole diam. and the no. of droplets generated per unit surface area of fluid film. Averaged over all film sizes, a higher surface tension yielded higher concns. of droplets. Surface tension did not influence the resulting droplet diam., but it was found that smaller films generated smaller droplets.Conclusions: This study shows that small fluid films generate droplets as efficiently as large films, and that droplets may well be generated from films with diams. below 1 mm. This has implications for the formation of film droplets from reopening of closed airways because human terminal bronchioles are of similar dimensions. Thus, the results provide support for the earlier proposed mechanism where reopening of closed airways is one origin of exhaled particles.
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    27. 27
      Johnson, G. R.; Morawska, L. The mechanism of breath aerosol formation. J. Aerosol Med. Pulm. Drug Delivery 2009, 22 (3), 229– 237,  DOI: 10.1089/jamp.2008.0720
      27
      The mechanism of breath aerosol formation
      Johnson Graham Richard; Morawska Lidia
      Journal of aerosol medicine and pulmonary drug delivery (2009), 22 (3), 229-37 ISSN:1941-2711.
      BACKGROUND: Aerosol production during normal breathing is often attributed to turbulence in the respiratory tract. That mechanism is not consistent with a high degree of asymmetry between aerosol production during inhalation and exhalation. The objective was to investigate production symmetry during breathing. METHODS: The aerosol size distribution in exhaled breath was examined for different breathing patterns including normal breathing, varied breath-holding periods, and contrasting inhalation and exhalation rates. The aerosol droplet size distribution measured in the exhaled breath was examined in real time using an aerodynamic particle sizer. RESULTS AND CONCLUSIONS: The dependence of the particle concentration decay rate on diameter during breath holding was consistent with gravitational settling in the alveolar spaces. Also, deep exhalation resulted in a four- to sixfold increase in concentration, and rapid inhalation produced a further two- to threefold increase in concentration. In contrast, rapid exhalation had little effect on the measured concentration. A positive correlation of the breath aerosol concentration with subject age was observed. The results were consistent with the breath aerosol being produced through fluid film rupture in the respiratory bronchioles in the early stages of inhalation and the resulting aerosol being drawn into the alveoli and held before exhalation. The observed asymmetry of production in the breathing cycle with very little aerosol being produced by exhalation is inconsistent with the widely assumed turbulence-induced aerosolization mechanism.
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    28. 28
      Galvani, A. P.; May, R. M. Dimensions of superspreading. Nature 2005, 438 (7066), 293– 295,  DOI: 10.1038/438293a
      28
      Epidemiology: Dimensions of superspreading
      Galvani, Alison P.; May, Robert M.
      Nature (London, United Kingdom) (2005), 438 (7066), 293-295CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)
      Analyses of contact-tracing data on the spread of infectious disease, combined with math. models, show that control measures require better knowledge of variability in individual infectiousness.
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    29. 29
      Lloyd-Smith, J. O.; Schreiber, S. J.; Kopp, P. E.; Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 2005, 438 (7066), 355– 359,  DOI: 10.1038/nature04153
      29
      Superspreading and the effect of individual variation on disease emergence
      Lloyd-Smith, J. O.; Schreiber, S. J.; Kopp, P. E.; Getz, W. M.
      Nature (London, United Kingdom) (2005), 438 (7066), 355-359CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)
      Population-level analyses often use av. quantities to describe heterogeneous systems, particularly when variation does not arise from identifiable groups. A prominent example, central to our current understanding of epidemic spread, is the basic reproductive no., R0, which is defined as the mean no. of infections caused by an infected individual in a susceptible population. Population ests. of R0 can obscure considerable individual variation in infectiousness, as highlighted during the global emergence of severe acute respiratory syndrome (SARS) by numerous superspreading events' in which certain individuals infected unusually large nos. of secondary cases. For diseases transmitted by non-sexual direct contacts, such as SARS or smallpox, individual variation is difficult to measure empirically, and thus its importance for outbreak dynamics has been unclear. Here we present an integrated theor. and statistical anal. of the influence of individual variation in infectiousness on disease emergence. Using contact tracing data from eight directly transmitted diseases, we show that the distribution of individual infectiousness around R0 is often highly skewed. Model predictions accounting for this variation differ sharply from av.-based approaches, with disease extinction more likely and outbreaks rarer but more explosive. Using these models, we explore implications for outbreak control, showing that individual-specific control measures outperform population-wide measures. Moreover, the dramatic improvements achieved through targeted control policies emphasize the need to identify predictive correlates of higher infectiousness. Our findings indicate that superspreading is a normal feature of disease spread, and to frame ongoing discussion we propose a rigorous definition for superspreading events and a method to predict their frequency.
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    30. 30
      Coleman, K. K.; Tay, D. J. W.; Sen Tan, K.; Ong, S. W. X.; Son, T. T.; Koh, M. H.; Chin, Y. Q.; Nasir, H.; Mak, T. M.; Chu, J. J. H.; Milton, D. K.; Chow, V. T. K.; Tambyah, P. A.; Chen, M.; Wai, T. K. Viral Load of SARS-CoV-2 in Respiratory Aerosols Emitted by COVID-19 Patients while Breathing, Talking, and Singing. Clin. Infect. Dis. 2021,  DOI: 10.1093/cid/ciab691
      There is no corresponding record for this reference.
    31. 31
      Group, f. t. U. o. M. S. R. Infectious SARS-CoV-2 in Exhaled Aerosols and Efficacy of Masks During Early Mild Infection. Clin. Infect. Dis. 2021,  DOI: 10.1093/cid/ciab797
      There is no corresponding record for this reference.

  • Supporting Information

    Supporting Information

    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.estlett.1c00760.

    • Details on data handling and statistical analyses and results of histogram of participants by age (Figure S1), description of testing facility and sampling schematic (Figure S2), signal-to-noise ratios for raw concentration data (Figure S3), correlation plots between respiratory aerosol emissions and participant voice volume (Figure S4) and measured CO2 mixing ratios (Figure S5), exhaled respiratory aerosol concentrations (Figure S6), plot of measured aerosol size distribution from singing (Figure S7), and outputs from linear models (Tables S1–S3) (PDF)


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